Air-breathing in vertebrates has evolved many times among the bony fish while in water. Its appearance has had a fundamental impact on the regulation of ventilation and acid-base status. We review the physico-chemical constraints imposed by water and air, place the extant air-breathing fish into this framework, and show how that the advantages of combining control of ventilation and acid-base status are only available to the most obligate of air-breathing fish, thus highlighting promising avenues for research.

Fish regulate ventilation primarily by sensing O2-levels in the water and arterial blood. It is well established that this sensory process involves several steps, but the underlying mechanisms remain frustratingly elusive. Here we examine the effect of increasing lactate ions at constant pH on ventilation in a teleost; specifically the facultative air-breathing catfish Pangasianodon hypophthalmus. At lactate levels within the physiological range obtained by Na-Lactate injections (3.5 ± 0.8 to 10.9 ± 0.7 mmol L−1), gill ventilation increased in a dose-dependent manner to levels comparable to those elicited by NaCN injections (2.0 µmol kg−1), which induces a hypoxic response and higher than those observed in any level of ambient hypoxia (lowest PO2 = 20 mmHg). High lactate concentrations also stimulated air-breathing. Denervation of the first gill arch reduced the ventilatory response to lactate suggesting that part of the sensory mechanism for lactate is located at the first gill arch. However, since a residual response remained after this denervation, the other gill arches or extrabranchial locations must also be important for lactate sensing. We propose that lactate plays a role as a signalling molecule in the hypoxic ventilatory response in fish.

It is well established that ectothermic vertebrates regulate a lower arterial pH when temperature increases. Typically, water-breathers reduce arterial pH by altering plasma [HCO], whilst air-breathers rely on ventilatory adjustments to modulate arterial PCO. However, no studies have investigated whether the shift from water- to air-breathing within a species changes the mechanisms for temperature-induced pH regulation. Here, we used the striped catfish Pangasianodon hypophthalmus to examine how pH regulation is affected by water- versus air-breathing, since P. hypophthalmus can accommodate all gas exchange by its well-developed gills in normoxic water, but achieves the same metabolic rate with aerial oxygen uptake using its the swim-bladder when exposed to aquatic hypoxia. We, therefore, measured arterial acid-base status in P. hypophthalmus as temperature changed between 20 and 35 °C in either normoxic or severely hypoxic water. In normoxic water, where P. hypophthalmus relied entirely on branchial gas exchange, P. hypophthalmus exhibited the typical teleost reduction in plasma [HCO] and arterial pH when temperature rose. However, when forced to increase air-breathing in hypoxic water, arterial PCO fell due to a branchial hyperventilation, but it increased with temperature most likely due to passive CO retention. We propose that the rise in arterial PCO reflects a passive consequence of the progressive transition to air breathing at higher temperatures, and that this response fortuitously matches the new regulated pH, relieving the requirement for branchial ion exchange.

No abstract

Lactate ions are involved in several physiological processes, including a direct stimulation of the carotid body, causing increased ventilation in mammals. A similar mechanism eliciting ventilatory stimulation in other vertebrate classes has been demonstrated, but it remains to be thoroughly investigated. Here, we investigated the effects of lactate ions on the cardiorespiratory system in swimming rainbow trout by manipulating the blood lactate concentration. Lactate elicited a vigorous, dose-dependent elevation of ventilation and bradycardia at physiologically relevant concentrations at constant pH. After this initial confirmation, we examined the chiral specificity of the response and found that only l-lactate induced these effects. By removal of the afferent inputs from the first gill arch, the response was greatly attenuated, and a comparison of the responses to injections up- and downstream of the gills collectively demonstrated that the lactate response was initiated by branchial cells. Injection of specific receptor antagonists revealed that a blockade of serotonergic receptors, which are involved in the hypoxic ventilatory response, significantly reduced the lactate response. Finally, we identified two putative lactate receptors based on sequence homology and found that both were expressed at substantially higher levels in the gills. We propose that lactate ions modulate ventilation by stimulating branchial oxygen-sensing cells, thus eliciting a cardiorespiratory response through receptors likely to have originated early in vertebrate evolution.